The Genomic History of Elephants Supports the Existence of a Third Modern Species and Has Important Implications for Conservation Kateryna Kratzer1

Home , African forest elephant, Palaeoloxodon

Proceedings of Manitoba’s Undergraduate Science and Engineering Research CC BY-SA 4.0 Kratzer, 2018, pmuser, 4(1): 87–89. DOI: 10.5203/pmuser.201841625 Review The Genomic History of Elephants Supports the Existence of a Third Modern Species and has Important Implications for Conservation Kateryna Kratzer1

1Dept. of Biological Sciences, University of Manitoba, Winnipeg, MB, R3T 2N2 Corresponding Author: K. Kratzer ([email protected])

Abstract African elephants have historically been classiﬁed as a single species. New research into the genomic history ofpro- boscideans has conﬁrmed that the African savanna elephant ( Loxodonta africana) and the African forest elephant ( Loxodonta cyclotis) are in fact distinct species. The depauperate genetic variability of L. africana which may be due to a bottleneck in their evolutionary history increases their species vulnerability. Loxodonta cyclotis is currently vulnerable and its numbers are in sharp decline. Reclassifying these elephants as distinct species would prove useful to future studies and promote unique conservation approaches for each species, which are likely necessary to prevent the further decline and potential extinctionof elephant populations.

Keywords: Proboscidean, Phylogeny, Species, Genetic Bottleneck, Conservation

1 Introduction distinct species, conservation efforts can be designed to ad- dress the specific needs of each species to ensure their ongo- he predecessors of modern elephants, such as ing preservation. Furthermore, updating the elephant fam- giant mammoths and mastodons, originated in ily tree to reflect accurate data will be useful for researchers Africa and roamed throughout much of North studying both ancient and modern proboscideans. America and Eurasia. Comprising 164 recognized The earliest proboscideans first appeared on the African Tspecies and subspecies1, these ancient proboscideans were continent between five and ten million years ago2, 1. These much more diverse than the modern species they gave rise creatures were relatively small and had short trunks1, al- to: the African elephant (Loxodonta africana) and its smaller though they would eventually give rise to the larger and more cousin the Asian elephant (Elephas maximus). From Carl recognizable modern elephants. The extant Asian elephant D. Illiger’s designation of elephants as Proboscidea in 18111 is clearly morphologically distinct from its African relatives up until very recently, these two were thought to be the with its shorter stature, smaller ears, elongated skull shape, only living proboscideans. However, according to genetic and straighter, more downward-facing tusks4. There are evidence, African elephants actually comprise two separate also notable differences between the two African species, al- species, bringing the total number of extant proboscidean though these have previously been insufficient to officially species up to three2. The African savanna elephant (Lox- recognize them as distinct. Loxodonta cyclotis is smaller, odonta africana) and the African forest elephant (Loxodonta has rounded ears, straighter and thinner tusks, and different cyclotis) should be classified as distinct species by conserva- skull morphology than its savanna-dwelling cousin5. In ad- tion organizations so that both unique groups may be pre- dition, the habitat of forest elephants is much smaller than served. The number of elephants in Africa was estimated to that of savanna elephants6. have decreased by between 104,000 and 114,000 from 2007 Distinguishing species based solely on morphology has to 2016 due to poaching and loss of habitat3. Despite the incorrectly dictated ideas of elephant evolutionary history. It World Wildlife Fund listing African forest elephants (des- was previously1 suggested that the Asian elephant was most ignated as a subspecies of African elephants) as vulnerable closely related to an extinct species called the straight-tusked and “in sharp decline”, there is no official estimate of their elephant (Palaeoloxodon antiquus) based on their morphol- population size. Updating the modern elephant family tree ogy, but recent work2 has shown that this is unlikely. This to include a third species is an important scientific advance- more precise classification of species, based not only on mor- ment with implications for both elephant conservation and phology but also on phylogeny and biology, led to two future study. By recognizing forest and savanna elephants as conclusions2: first that the most recent common ancestors

Frontiers of Undergraduate Research 88 pmuser, 2018, 4(1)

mitochondrial diversity were used to construct phylogenetic trees, which gave overviews of the relationships between the genomes. This and other genetic studies of modern and extinct elephants provide two points of compelling evidence for the existence of two distinct species in Africa. First, there is no significant gene flow between modern African forest and savanna elephants2, 6, 9, although there was considerable interbreeding between ancient elephant species2. The two types of elephants currently living in Figure 1: Revised tree of phylogenetic relationships among elephant Africa are therefore arguably more distinct than their ancient species based on straight-tusked elephant genome analysis. Branch relatives, which are classified as separate species. lengths are not proportional to time. Data from Meyer et al.֥ Second, despite having a smaller geographic range6 and (mrcas) are different than previously determined, and sec- therefore less opportunity to accumulate genetic diversity, ond that there are three extant elephant species. African ele- forest elephants are more genetically diverse than their sa- phants should therefore be officially recognized as two dis- vanna counterparts5. Genetic samples from savanna ele- tinct species based on their morphology, phylogeny, and bi- phants were nearly identical5, indicating a genetic bottleneck ology. event in their past. Bottlenecks decrease genetic variability in a species and can be extremely detrimental to species sur- vival. Lack of genetic variation in other African animals such 2 The Elephant Family Tree as the cheetah (Acinonyx jubatus jubatus) can lead to diffi- culty breeding in captivity, high rates of juvenile mortality, Of the 164 recognized proboscidean species1, only two were spermatozoal abnormalities, and increased vulnerability to believed to be extant. However, Shoshani1 acknowledged zoonotic diseases10. These factors are important considera- that there may be three living species of elephants, and later tions for the field of conservation biology as they can com- studies outlined by Grubb et al.8 suggested that African plicate efforts to conserve threatened species. forest and savanna elephants should be classified separately based on morphology. This evidence was insufficient to justify the separate classification of African species. A re- 4 Conclusion cent phylogenetic tree (Fig. 1) based on genomic analysis of P. antiquus7 recognized separate African species. This was Proving the existence of two African elephant species has im- confirmed2 by performing genetic analysis on samples from portant implications for immediate conservation efforts as a variety of living and extinct proboscideans. well as future scientific research. The classification of for- The MRCA of the extinct straight-tusked elephant and est and savanna elephants as separate species will directly im- the African forest elephant lived closer to modern times than pact conservation and management approaches by promot- did the MRCA of both modern African species (Fig. 1). ing individualized efforts to protect each species as a distinct The forest elephant is therefore more closely related to P. group. Widely accepted data that accurately depicts the rela- antiquus than it is to the concurrent savanna elephant. In tionships between modern and extinct elephant species will fact, L. africana and L. cyclotis have been genetically isolated, allow for more consistent data collection in the future, fur- meaning there has been no genetic exchange between their thering our biological understanding of the past and present. ancestors, for approximately 500,000 years2. Since the two The loss of a subspecies is not as devastating as the ex- African species diverged earlier in history than the forest ele- tinction of an entire species. Organizations such as IUCN phant and the straight-tusked elephant, they have been ge- and the World Wildlife Fund can focus their efforts on sav- netically distinct species for a long period of time. ing both African elephant species from extinction if they recognize them as such, rather than classifying L. cyclotis as a subspecies of African elephant. Unique conservation efforts 3 Modern Elephant Genetics directed towards each species are important2, 7, 6, 9. Despite the vulnerability of forest elephants in particular, the offi- Palkopoulou et al.2 sequenced the genomes of 14 pro- cial census3 paints a grim picture for all remaining elephants boscideans and aligned them to a reference genome from an in Africa, making them a broad priority for conservation ef- extant African savanna elephant. Different molecular fea- forts. Separate studies of forest and savanna elephants are tures of the data such as divergence between nucleotides and required in order to better understand these unique animals

Frontiers of Undergraduate Research Kratzer 89 and shape conservation approaches tailored to each. A wider Africa; L. africana, the savanna elephant, and L. cyclotis, the approach, based on the old single African species idea, could forest elephant. They differ in their morphology, phylogeny, result in the loss of one or both African elephant species. and biology. The two types have been genetically distinct Using our current knowledge of each species ecology, for half a million years and show different levels of genetic we can begin to identify better conservation approaches. diversity. They should therefore be recognized as separate African forest elephants live in dense vegetation and are species. Additional genomic analysis of ancient specimens therefore difficult to identify and study without specialized can help further unravel the past while the recognition of techniques such as thermal imaging11. More comprehensive distinct African elephant species will shape current studies study of these elusive animals requires the use of techniques and conservation efforts, thereby helping save more elephant and technologies that are customized to their behaviour. Sa- species from extinction. Genetic study is vital to the field of vanna elephants are easier to observe in their open habitat biology in terms of the past, present, and future. but likely require different conservation approaches due to their limited genetic variation. Careful breeding programs to prevent any further decrease in savanna elephant genetic References diversity would not be applicable to the more genetically diverse forest elephant populations. Interbreeding between 1. Shoshani, J. 1998. Trends in Ecology & Evolution, 13: 480– the two species, which may occur if they are housed together 487. in captivity under the assumption of belonging to a single 2. Palkopoulou, E., Lipson, M., Mallick, S., et al. 2018. Proceedings of the National Academy of Sciences of the United species, would destroy any genetic differences between the States of America. species. If these species are not conserved separately, we may 3. Thouless, C., Dublin, H., Blanc, J., et al. 2016. IUCN, end up losing both. 60: 1–10. In addition to the importance this has in regard to ele- 4. Todd,N. 2010. The Anatomical Record, 293: 62–73. phant conservation, accurate genetic data is critical to gen- 5. Roca, A., Georgiadis, N., Pecon-Slattery, J., et al. eral scientific inquiry and knowledge. An updated elephant 2001. Science, 293: 1473–1477. family tree will help guide future molecular studies on ge- 6. Mondol, S., Moltke, I., Hart, J., et al. 2015. Molecular Ecology Resources, 24: 6134–6147. netics and genomic histories, as well as more traditional bi- 7. Meyer, M., Palkopoulou, E., Baleka, S., et al. 2017. ological studies on the behaviour, distribution, and popu- eLife, 6: e25,413. lation changes of African forest and savanna elephants. In 8. Grubb, P., Groves, C., Dudley, J., et al. 2000. Elephant, 2: addition, the techniques used2 to determine historical rela- 1–4. tionships between proboscidean genomes can be applied to 9. Roca, A., Ishida, Y., Brandt, A., et al. 2015. Annual Re- broader studies on the genomic history of other species. view of Animal Biosciences, 3: 139–167. The history of elephants is more interesting and compli- 10. O’Brien, S., Roelke, M., Marker, L., et al. 1985. Science, cated than once thought. Two species of elephants reside in 227: 1428–1434. 11. Clabby, C. 2012. American Scientist, 100: 416–417.

Frontiers of Undergraduate Research